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Reproductive Biology |
2Departamento de Botânica, Universidade Federal do Rio de Janeiro, CCS, IB, CEP 21941-590, Rio de Janeiro-RJ, Brazil; 3Departamento de Ecologia, Universidade Federal do Rio de Janeiro, CCS, IB, Caixa Postal 68020, CEP 21941-590, Rio de Janeiro-RJ, Brazil
Received for publication November 23, 2004. Accepted for publication June 17, 2005.
ABSTRACT
We examined the frequency of hermaphroditic, monoecious, and dioecious species of angiosperms in restinga (sandy coastal plain) vegetation in SE Brazil. The study site was a vegetation mosaic comprising nine plant formations, ranging from open types to forest. Dioecy (14% of 566 species) was similar to other tropical vegetations and strongly associated with woodiness and entomophily. However, more interestingly, there was an exceptionally high percentage (35%) of dioecious species among the dominant woody plants. This pattern has not been previously reported, and we discuss the extent to which it is ecologically driven. We argue that the high abundance of dioecious plants in this resource-poor environment can be attributed to ecological traits related to long-distance dispersal, ecological vigor, and possibly, vegetative reproduction.
Key Words: dioecy • monoecy • resource-poor environments • restingas • sandy coastal plains • sexual systems
Significant efforts have been made to understand the wide variety of breeding systems in angiosperms, which ranges from almost obligate selfing to obligate out-crossing, and from self-incompatibility to dioecism (Darwin, 1877
; Bawa, 1980
; Bawa and Beach, 1981
; Lloyd, 1982
; Endress, 1994
). While hermaphroditism is the dominant condition in flowering plants (Renner and Ricklefs, 1995
), diclinous systems such as monoecy and dioecy have been studied in an effort to understand the evolution of unisexual systems and the significance of these systems within the angiosperms (Weller and Sakai, 1999
; Weiblen et al., 2000; Vamosi et al., 2003
; Vamosi and Vamosi, 2004
).
The evolution of unisexual systems has often been related to the fact that outcrossing avoids the consequences of inbreeding depression (Charlesworth and Charlesworth, 1978
; Thomson and Barrett, 1981
; Lloyd, 1982
; Sakai et al., 1995a
; Freeman et al., 1997
). Moreover, dioecy has been correlated with plant spatial distribution, tropical floras, oceanic islands, and oligotrophic environments (Freeman et al., 1976
; Bawa, 1980
; Flores and Schemske, 1984
; Bawa et al., 1985
; Sakai et al., 1995a
, b
; Thompson and Edwards, 2001
), and since Darwin (1877)
, resource allocation has been suggested as a causal factor in the evolution and maintenance of dioecy.
Dioecy has also been correlated with a number of ecological attributes (Bawa and Opler, 1975
; Bawa, 1980
; Flores and Schemske, 1984
), such as woodiness (Croat, 1979
; Bawa et al., 1985
; Bullock, 1985
; Ormond et al., 1991
; Sakai, 1995b
; Oliveira, 1996
), climber habit (Renner and Ricklefs, 1995
), entomophily (Bawa, 1974
; Ibarra-Manríquez and Oyama, 1992
; Oliveira and Gibbs, 2000
; but see Renner and Feil, 1993
), anemophily (Givnish, 1980
), and formation of fleshy fruits dispersed by animals (Givnish, 1980
; Ibarra-Manríquez and Oyama, 1992
). Recent large-scale molecular phylogenetic analyses confirm some of the correlations between dioecy and ecological traits and highlight the diversification of dioecious lineages associated with ecological features such as the ones listed (Weller and Sakai, 1999
; Vamosi et al., 2003
).
The correlation between dioecy and ecological attributes and/or types of habitats has often been established based on surveys of sexual systems for entire floras (e.g., Croat, 1979
; Steiner, 1988
) or restricted to certain areas or plant life forms (e.g., Bawa and Opler, 1975
; Oliveira, 1996
). In this study, we aimed to correlate sexual systems with ecological attributes for Brazilian sandy coastal plain vegetation, locally called restinga. The restinga vegetation is a mosaic of plant communities consisting of halophytic beach vegetation, open shrubby formations, and dry and swamp forest (see Lacerda et al., 1993
). It grows on sandy marine deposits dating from the Quaternary, which separate the sea from the Tertiary-age rainforest on the neighboring mountain range (Scarano, 2002
). Araujo (2000)
has shown that there are very few endemic plants in the restinga and that ca. 80% of the species are originally from the Atlantic rainforest. Because restingas, like most coastal ecosystems, subject plants to a myriad of stressful conditions (e.g., oligotrophy, drought, salinity, high temperature, flooding), it has been argued that adaptation of many rainforest plants to these habitats indicates high ecological plasticity (see review in Scarano, 2002
).
In summary, restingas are (1) resource-poor environments, (2) a vegetation mosaic ranging from creeping herbaceous to forest communities, and (3) geologically young and newly colonized by neighboring rainforest plants. Thus, we have chosen this vegetation type to test predictions that dioecy is related to resource-poor environments and to woodiness, by assessing the frequency of hermaphroditic, monoecious and dioecious species (totaling 566) for each of nine plant formations at our study site. Moreover, we also assessed how sexual system type related to phytosociological dominance for woody species of three specific, conspicuous plant formations, and to pollinator syndrome and fruit type. Phytosociological dominance is a measure of abundance, and we found no literature relating this ecological property to sexual system type. The fact that restingas are geologically young and have a flora composed mostly of migrants from neighboring rainforest raised the expectation that there would be a small proportion of dioecious species among the dominants. Hermaphroditic selfing plants are expected to be favored during colonization, because one seed produced in one plant is potentially capable of establishing a new population (Stebbins, 1957
). Dioecious plants would depend predominantly on vectors for cross-pollination and it appeared improbable that pollination-vectors would follow the migration of plant species from a mesic forest to harsh coastal environment (Lopes and Machado, 1998).
MATERIALS AND METHODS
Study site
This survey was conducted at the Restinga de Jurubatiba National Park (RJNP) located on the northern coast of Rio de Janeiro State, SE Brazil (22°00'–22°23' S, 41°15'–41°35 W) within the municipalities of Macaé, Carapebus, and Quissamã. Restingas cover most of the 5000 km of Brazilian coastlines. The RJNP protects an area of 14 480 ha and 44 km of coast, with a series of parallel Pleistocene-age beach ridges and brackish coastal lagoons, formed when ancient river deltas were obstructed by the silting of marine sediments (Henriques et al., 1986
). This restinga comprises nine different vegetation physiognomies (Araujo et al., 1998
; see Table 1). The patchy vegetation dominated by Clusia hilariana trees covers ca. 40% of the park. Rainfall is seasonally distributed, with minimum monthly values (41 mm) and soil water deficit during the winter (June to September) and maximum (189 mm) during the summer (December to February). Mean annual temperature is 22.6°C, mean maximal annual temperature is 29.7°C in January and mean minimal is 20.0°C in July (Henriques et al., 1986
). The flora is relatively rich (Costa and Dias, 2001
), which is quite surprising given the shortage of resources available to plants and the frequent exposure to extreme abiotic conditions.
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) with additions from other surveys (Montezuma, 1997
; Zaluar, 1997
; Araujo et al., 1998
, 2000
, 2004
; Oliveira, 2000
). We excluded from the analysis all nonindigenous species (30 spp.), unidentified specimens (34 spp.), as well as those lacking information on habitat type within the RJNP (26 spp.), or sexual system type (11 spp.). Our final list totaled 566 angiosperm species (Appendix S1, see Supplemental Data with online version of this article).
We also prepared a list of the dominant woody species based on previous studies for the three most representative plant formations locally as regards area covered: (1) the open Clusia scrub, (2) the open Ericaceae scrub, and (3) the periodically flooded forest (Montezuma, 1997
; Oliveira, 2000
; Araujo et al., 2004
). These three communities harbor almost 90% of the woody species recorded for the study site (Araujo, 2000
). We classified as dominants 43 woody species (Table 2), each with its reported importance value (IV) >1. The IV is a phytosociological index obtained from the sum of relative frequency, relative basal area, and relative density (Müller-Dombois and Ellenberg, 1974
). It is a comparative measure of species dominance within communities.
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, and genera and species were checked with the nomenclature databases w3Tropicos (http://mobot.mobot.org/W3T/Search/vast.html, accessed 15 June 2005) and The International Plant Names Index (http://www.ipni.org/index.html, accessed 15 June 2005).
Sexual systems
Species were classified as hermaphrodites when bisexual flowers were present, monoecious when separate male and female flowers (unisexual) were present on the same individual, and dioecious when female and male flowers were present on different individuals (Bawa, 1980
; Endress, 1994
). Polygamous species described as gynodioecious and androdioecious were considered dioecious; and gynomonoecious and andromonoecious were listed as monoecious, because perfect flowers in these species are often functionally unisexual (Bawa, 1980
; Flores and Schemske, 1984
). Characterization of floral sexuality was largely based on a meticulous literature search of published floras (Martius et al., 1840–1906
; Reitz, 1965–1989
; Reis, 1996–1997
). We also consulted taxonomists, examined herbarium vouchers from Brazilian restinga collections deposited at the Rio de Janeiro Federal University Herbarium (RFA), and performed field observations from November 2002 to February 2003.
Comparison with other floras
We compared the frequencies of hermaphroditic, monoecious, and dioecious species in our study site (whole flora and dominant woody species only) with several other floras reported in the literature (Table 3). Polygamous species (4%) recorded by Croat (1979)
were excluded for comparative purposes, because we could not discriminate them as monoecious or dioecious following the criteria used in our study.
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Plant communities
We surveyed the habitat preferences for 566 species belonging to all nine plant communities (Table 1) and scored the frequencies of hermaphroditic, monoecious, and dioecious species for each of these communities.
Pollination and fruit type
We evaluated pollination and fruit type for the 43 dominant woody species. Information on pollination syndromes and fruit types were recorded based on the literature (Reitz, 1965–1989
; Bawa, 1980
; Ormond et al., 1991
; Endress, 1994
; Reis, 1996–1997
; Judd et al., 1998
). Fleshy fruits were defined as fruits with a fleshy pericarp, or with a dry pericarp where seeds are embedded in a fleshy pulp or attached to an aril (Flores and Schemske, 1984
).
Data analysis
The distribution of hermaphroditism, monoecy, and dioecy according to life-forms, plant communities, pollination syndromes, and fruit type were compared by chi-square tests using STATISTICA version 6.0 for Windows (Statsoft, 1996). The null hypothesis for all comparisons was that the frequency distribution of sexual systems in the various categories was not significantly different from the distribution for the entire flora or for the dominant woody species, respectively.
RESULTS
Sexual systems
Of the total of 566 species recorded in this survey, 428 (75%) were hermaphroditic, 78 (14%) were dioecious, and 60 (11%) were monoecious. Of 108 families recorded in the flora, 67% were exclusively hermaphroditic, 11% were exclusively dioecious (Clusiaceae, Dioscoreaceae, Aquifoliaceae, Polygonaceae, Smilacaceae, Burseraceae, Simaroubaceae, Ebenaceae, Meliaceae, Celastraceae, Dilleniaceae, and Menispermaceae), and 6% were exclusively monoecious (Arecaceae, Alismataceae, Cecropiaceae, Ceratophyllaceae, Typhaceae, and Ulmaceae). All exclusively monoecious families were represented by only one species. The remaining 15% were families with hermaphroditic and monoecious species (N = 4), hermaphroditic and dioecious species (N = 5), monoecious and dioecious species (N = 5), or a combination of all three sexual systems, which was present only in the Cyperaceae. Unisexual species were present in 21% of the genera: 38 were dioecious and 37 monoecious. Genera were often exclusively of one type of sexual system. Appendix S1 (in online Supplemental Data) provides a full list of species names and respective families, sexual systems, life forms and habitat types in the Restinga de Jurubatiba National Park.
The percentage of dioecious species (35%) among the 43 dominant woody plants of the three most representative plant communities was exceptionally high (Table 2). Ten of the 27 dominant woody species in the open Clusia scrub were dioecious (37%), including the most abundant species, Clusia hilariana and Protium icicariba. Similarly, five of the 12 dominant woody species (41.6%) in the open Ericaceae scrub (e.g., P. icicariba and C. hilariana) and eight of the 18 species (44.4%) in the periodically flooded forest were dioecious (e.g., Tapirira guianensis, Symphonia globulifera, and Calophyllum brasiliense). The periodically flooded forest was the only one of the three important formations to have monoecious species with considerably high abundance (e.g., Geonoma schottiana). Note that some of the dominant woody species were dominant in more than one of the three formations: two species (Tapirira guianensis and P. icicariba, both dioecious) were common to all three habitats, eight species (three of which are dioecious) were common to Clusia scrub and Ericaceae scrub; and only one species was common to Clusia scrub and periodically flooded forest, and another one was common to Ericaceae scrub and periodically flooded forest (Table 2).
Comparison with other floras
Frequency distribution of sexual systems for the 566 restinga species was comparable to other Brazilian floras (Table 3). The flora of the Maricá restinga had a similar proportion of hermaphrodites, whereas monoecy was more frequent and dioecy less frequent. Proportions were also strikingly similar to those found in the neighboring Atlantic rainforest at Macaé de Cima, and the savanna in central Brazil. Values were generally similar elsewhere in the tropics, with the exception of a dipterocarp forest in Malaysia and a semi-deciduous forest in Costa Rica, where dioecy was particularly high, and a swamp forest in Venezuela where dioecy was particularly low. However, the relative frequency of dioecy (35%) among dominant woody species at our restinga site was exceptionally high, greater than all other examples we found in the literature (Table 3).
Association of sexual system with life form
Trees and shrubs (woody species) were 45% (254) of the flora at the study site. Herbs represented 39% (214) and climbers 16% (98) (Table 4). The woody species included proportionately more dioecious species (22%; 57), and herbs had proportionately fewer dioecious species than expected from a random distribution (4%; 8), resulting in a strongly significant association between dioecy and woody life forms (
2 = 31.3, P < 0.0001; Table 4). Similarly, distribution of hermaphroditic herbs was proportionately higher than expected and that of trees, shrubs and climbers was lower than expected, also showing a positive association between herbs and hermaphroditism (2 = 8.5, P < 0.05; Table 4).
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The frequency distribution of sexual systems recorded at the restinga site is generally comparable to other tropical forests, deciduous forests, and savannas. The high percentage of dioecy recorded (14%), greater than the estimate for the entire angiosperm flora (6%, Renner and Ricklefs, 1995
), agrees with the notion that unisexual systems are strongly correlated with tropical environments (Bawa, 1974
, 1980
; Bawa and Opler, 1975
; Flores and Schemske, 1984
; Renner and Ricklefs, 1995
). More interestingly, however, dioecious species represented 35% of the dominant woody species of the three most representative vegetation types in the area. Thus, we have divided this section into two parts where we discuss (1) the patterns found for the entire local flora and (2) the patterns found for the dominant woody species of these three common vegetation types.
Patterns detected for the entire local flora
Sexual systems and life forms
The positive correlation between dioecy and tropical environments has been attributed to the fact that tropical climates favor the woody habit (Bawa, 1980
; Givnish, 1980
) and dioecy, in turn, is strongly related to woodiness (e.g., Ibarra-Manríquez and Oyama, 1992
). In our study, 36% of all tree and shrub species were dioecious.
This association between dioecy and woodiness is also seen as a result of a strong selection for outcrossing in plants with a long life span (Bawa, 1980
; Sakai et al., 1995b
). Indeed, woody species with a long life span, tend to have restricted recombination, and consequently, it is more probable that they are selected for outbreeding, as compared to short-lived plants (Stebbins, 1950
; Steiner, 1988
).
Unisexual systems and oligotrophic environments
Darwin (1877)
was the first to suggest that separate sexes were favored in stressful environments. Models and empirical surveys explaining the evolution and maintenance of diclinous taxa later supported this assumption (Bawa and Opler, 1975
; Freeman et al., 1997
; Thompson and Edwards, 2001
). Division of labor in unisexual plants may increase male and female fitness due to a compensation effect (e.g., Lloyd and Webb, 1977
; Sutherland and Delph, 1984
), unless physiological constraints are so severe as to generate low plant density or lack of pollinators or reduced fertility. In the restinga habitats where dioecy was abundant, nutrient shortage is the main feature. While in flooded forests oxygen availability for roots is much reduced during flooding (e.g., Scarano et al., 1997
), in the open scrubs water and nutrient shortage are common features of the sandy soils (e.g., Liebig et al., 2001
)
Patterns detected for the dominant woody species
For the 43 dominant woody species recorded for three most representative plant communities, we found an exceptionally high proportion of dioecious plants (35%). It seems paradoxical that the dominant plant species of a geologically young habitat, such as this restinga, would depend predominantly on vectors for cross-pollination, since it appears improbable that pollination-vectors would follow the migration of plant species from a mesic forest to a harsh coastal environment. For instance, we studied the reproductive biology of the most abundant plant in the open Clusia scrub, C. hilariana, and found that despite high abundance this species has a low success of sexual reproduction locally (Metallana et al., A. Faria, Universidade Federal do Rio de Janeiro, unpublished data). We think that vegetative propagation (since no apomixis was found) was partly responsible for the plant's high abundance, following Baker and Cox (1984)
who have argued that this "dioecy handicap" may be overcome by such asexual reproductive strategy.
On the other hand, we found that dioecy was strongly associated with generalist entomophily. Bawa (1982)
suggested that generalist pollinators allow dioecious plants to establish more readily than hermaphrodites that require specialist pollinators. Charlesworth (1993)
also hypothesized that dioecy may evolve more easily if pollination mechanisms, such as wind or small insects, do discriminate female flowers from hermaphroditic flowers with pollen rewards.
Moreover, although no statistically significant association was found, fleshy fruits (suggesting biotic dispersal) are important features of the dominant woody species at our study site. Since sex separation might imply enhanced female fitness with the production of attractive fruits, this may further assure successful dispersal of propagules by birds or mammals. Indeed, previous evidence indicates that tropical distribution of dioecy is positively correlated with fleshy fruits (Weller and Sakai, 1999
; Vamosi et al., 2003
; Vamosi and Vamosi, 2004
), which are often dispersed by birds and have twice the sib-competition because seeds disperse only around females in populations where plant sexes are separated (Heilbuth et al., 2001
). Because fleshy fruits are related to long-distance dispersal, and most of the local flora is composed of plants that migrated from the neighboring Atlantic rainforest (Araujo, 2000
; Scarano, 2002
), this could partly explain the high abundance of dioecious plants at the study site.
Concluding remarks
Our results confirm most of the expected patterns for dioecy in tropical vegetation extensively reported in the literature. In our restinga site, dioecy has been strongly associated with woodiness, generalist entomophily, and resource-poor environments. However, the strong association between dioecy and phytosociological dominance has not been previously reported and clearly indicates the relevance of ecological traits. Although it remains to be seen to which extent phylogenetic origin interferes with the patterns found (see Vamosi et al., 2003
), long-distance dispersal of predominantly fleshy fruits of the dioecious species and ecophysiological vigor in the oligotrophic restingas (e.g., Scarano et al., 2005) are most likely related to fitness and local success of such species. It also remains to be seen how other traits commonly associated with dioecy, such as vegetative reproduction (see Baker and Cox, 1984
), contribute to such a high abundance of dioecious plants in the flora. Vegetative reproduction, through clonal growth or resprouting, is a typical feature of many restinga plants (e.g., Cirne and Scarano, 2001
; Scarano et al., 2002
; Cirne et al., 2003
; Sampaio et al., 2004
).
FOOTNOTES
1 The authors thank P. E. Gibbs and L. Freitas for valuable discussions on the subject; C. H. DePaula, M. Gomes, H. C. de Lima, R. C. Lopes, S. Potsch, and A. Quinet for kindly providing specialist information about taxonomy and sexual system of several plant families; M. J. Barros for assistance during the early stages of this study; the Brazilian Long-Term Ecological Research Program (LTER), site 5 (PELD/CNPq) for funding; G. K. Brown for linguistic advice; two anonymous reviewers for useful comments on the manuscript; and the Brazilian Research Council (CNPq) for grants to the authors. This paper is part of a Master's thesis at the Post-Graduate Programme in Ecology of the Universidade Federal do Rio de Janeiro by G.M. 
4 Author for correspondence (e-mail: twendt{at}biologia.ufrj.br
)
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